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Hassan, O A., Affognon, H., Rocklöv, J., Mburu, P., Sang, R. et al. (2017)The One Health approach to identify knowledge, attitudes and practices that affect communityinvolvement in the control of Rift Valley fever outbreaks.PLoS Neglected Tropical Diseases, 11(2): e0005383https://doi.org/10.1371/journal.pntd.0005383
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RESEARCH ARTICLE
The One Health approach to identify
knowledge, attitudes and practices that affect
community involvement in the control of Rift
Valley fever outbreaks
Osama Ahmed Hassan1,2*, Hippolyte Affognon3,4, Joacim Rocklov5, Peter Mburu3,
Rosemary Sang3, Clas Ahlm6, Magnus Evander1
1 UmeåUniversity, Clinical Microbiology, Virology, Umeå, Sweden, 2 Public Health Institute, Khartoum,
Sudan, 3 International Centre of Insect Physiology and Ecology, Nairobi, Kenya, 4 International Crops
Research Institute for the Semi-Arid Tropics (ICRISAT), Bamako, Mali, 5 UmeåUniversity, Public Health and
Clinical Medicine, Epidemiology and Global Health and UmeåCentre for Global Health Research, Umeå,
Sweden, 6 UmeåUniversity, Clinical Microbiology, Infectious Diseases, Umeå, Sweden
Abstract
Rift Valley fever (RVF) is a viral mosquito-borne disease with the potential for global expan-
sion, causes hemorrhagic fever, and has a high case fatality rate in young animals and in
humans.
Using a cross-sectional community-based study design, we investigated the knowledge,
attitudes and practices of people living in small village in Sudan with respect to RVF out-
breaks. A special One Health questionnaire was developed to compile data from 235 heads
of household concerning their knowledge, attitudes, and practices with regard to controlling
RVF. Although the 2007 RVF outbreak in Sudan had negatively affected the participants’
food availability and livestock income, the participants did not fully understand how to identify
RVF symptoms and risk factors for both humans and livestock. For example, the participants
mistakenly believed that avoiding livestock that had suffered spontaneous abortions was the
least important risk factor for RVF. Although the majority noticed an increase in mosquito
population during the 2007 RVF outbreak, few used impregnated bed nets as preventive
measures. The community was reluctant to notify the authorities about RVF suspicion in live-
stock, a sentinel for human RVF infection. Almost all the respondents stressed that they
would not receive any compensation for their dead livestock if they notified the authorities. In
addition, the participants believed that controlling RVF outbreaks was mainly the responsibil-
ity of human health authorities rather than veterinary authorities. The majority of the partici-
pants were aware that RVF could spread from one region to another within the country.
Participants received most their information about RVF from social networks and the mass
media, rather than the health system or veterinarians. Because the perceived role of the com-
munity in controlling RVF was fragmented, the probability of RVF spread increased.
PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0005383 February 16, 2017 1 / 12
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OPENACCESS
Citation: Hassan OA, Affognon H, Rocklov J,
Mburu P, Sang R, Ahlm C, et al. (2017) The One
Health approach to identify knowledge, attitudes
and practices that affect community involvement in
the control of Rift Valley fever outbreaks. PLoS
Negl Trop Dis 11(2): e0005383. doi:10.1371/
journal.pntd.0005383
Editor: Brian Bird, School of Veterinary Medicine
University of California Davis, UNITED STATES
Received: August 3, 2016
Accepted: February 3, 2017
Published: February 16, 2017
Copyright: © 2017 Hassan et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: The study was supported by the Swedish
International Development Cooperation Agency
and the Swedish Research Council. The first author
(OAH) was supported by a research scholarship
from Umeå Centre for Global Health Research, and
the Medical Faculty of Umeå University. The
funders had no role in study design, data collection
Author summary
Rift Valley fever (RVF), is a neglected, emerging, mosquito-borne disease that has caused
outbreaks in Africa and the Arabian Peninsula. RVF outbreaks have a severe negative
impact on livestock, human health and economy, placing further demands on communi-
ties already experiencing high levels of poverty. We believe there is an immediate need to
develop new approaches that will tackle the ongoing spread of RVF. One such approach
would prioritize outbreak prevention by involving local communities in the surveillance
of emerging zoonotic diseases, empowering local communities as agents of change rather
than relegating them as passive victims. RVF is a disease with global implication, but it
starts at a local level. Therefore, to control zoonotic disease such as RVF, it is important to
understand the local communities’ knowledge, attitudes and practices related to RVF.
Using a bottom-up perspective, we investigated the factors that keep the local community
from participating in the control of RVF outbreaks at the interface between humans, ani-
mals, and the environment. By devising acceptable and cost-effective interventions, we
believe local communities can be encouraged to be the first line of defense against RVF
outbreaks. Furthermore, policies aimed at curtailing RVF outbreaks would benefit from
involvement of the local communities.
Introduction
Global outbreak of zoonotic infections, not only affect human and animal health but also affect
food security, and socio-economic stability. To control such outbreaks require local as well
regional cooperation. Most zoonotic outbreaks begin and occur in settings where resources
are poor and where the outbreak severely affect the local community [1, 2]. These outbreaks
spread both within and outside the country of origin, often with devastating consequences [3].
Zoonotic infections originate and spread at the interface between humans, animals, and their
environments, making them candidates for the One Health approach to disease control [4–8].
Although international organizations, government authorities, and academic institutions,
believe the One Health concept should be a part of a local community’s response to zoonotic
infection, the One Health concept is rarely implemented at the community level. It is undeni-
able that community involvement is crucial in reducing the risk of zoonotic diseases at the
interface between animal-human and their ecosystem.
Rift Valley fever (RVF) is a mosquito-borne viral disease affecting both humans and ani-
mals. It can be transmitted by mosquito bites or by direct contact with infected animals, their
fluids, or products derived from them [9]. The disease in humans varies from a mild influ-
enza-like illness to more severe forms such as hemorrhagic fever, renal failure, encephalitis,
retinitis and miscarriage [9, 10]. Because there is no approved human vaccine or treatment
available for RVF, RVF poses a major threat to public health [9]. The infection causes so called
“abortion storm” in livestock and deadly epidemics in young animals, with severe conse-
quences for local and national economies [11]. RVF is present in Africa, and as of 2000, it has
spread to the Arabian Peninsula [12, 13]. Environmental changes, international travel, trade,
and the spread of RVF virus (RVFV) and vectors outside of Africa highlights the potential for
its global spread [14–17].
Sudan is an agricultural country with diverse ecology and has the second largest livestock
population in Africa. Most of the Sudanese population depends on livestock for food and
income. Our previous studies of the RVF 2007 outbreak in Sudan found a gap in knowledge
regarding the role of the local community [2, 18]. In this study, we used a bottom-up approach
Rift Valley fever outbreak control
PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0005383 February 16, 2017 2 / 12
and analysis, decision to publish, or preparation of
the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
to evaluate the knowledge, attitudes and practices that affect how the local agro-pastoralist
community in Sudan confronts an RVF outbreak.
Methods
Study area, population, and design
In accordance with the guidelines of strengthening and reporting of observational studies in
epidemiology (STROBE), a cross-sectional community-based study was conducted in March
2013 at the Mabroka Sagadi village in the Managil locality, Gezira State, Sudan (Fig 1).
The Managil locality is close to irrigation canals. The local people are mainly farmers and
shepherds and the locality is home to about 2 million livestock (mainly cattle, sheep and
goats). The annual rainfall in the region varies between 100 and 350 mm; however, in 2007 the
rain level reached up to 400 mm [19]. The rainy season is from mid-June to September. Mana-
gil is located in the Savannah zone and the temperature ranges from 25˚C to 46˚C.
The study area included all the states affected by the 2007 RVF outbreak (Fig 1). Most of the
reported human cases (n = 402) [20] were found in Gezira, so this state was selected. In Gezira,
the Managil locality reported the highest number of cases and the village of Mabroka Sagadi
had nine recorded human RVF cases during the 2007 outbreak. At the time of the study, there
were 5,830 inhabitants in Mabroka Sagadi village. Of the 641 households in the village, 240
households were randomly selected, with a response rate of 98% (n = 235). The household
head was defined as the person who in charge of the household and any dependents. We inter-
viewed the household heads and all of them were men or women at least 15 years of age.
Pilot study and validation of questionnaire
To develop the One Health questionnaire to collect data about RVF at the human-animal-envi-
ronment interfaces, we intensively searched the literature for information that would help us
develop questions regarding the disease and we searched for the best possible answers to these
questions supported by the medical literature. This research resulted in the One Health ques-
tionnaire that was designed to compile relevant data on RVF in humans, animals, and the envi-
ronment. Originally written in English, the questionnaire was eventually translated into Arabic
(S1 Table). The questions were open ended and the participants were allowed to provide more
than one answer. The participants’ answers were compared to the answers listed in the ques-
tionnaire but these answers were hidden from the participants to avoid leading questions. If the
participant’s answer was not in the listed answers, it was added to the category named “other”.
A two-day training workshop was held for data collectors (public health officers acquainted
with the study area) to discuss the objectives of the study, the contents of the questionnaire,
and the methods of the study.
A pilot study was conducted in the village of Algila (Fig 1). Algila had similar socio-cultural
and ecological characteristics to those of the final study area, and it was also affected by the
2007 RVF outbreak. The findings were analyzed and used to update the questionnaire for the
full-scale study.
Data collection and analysis
A pre-study field visit to the study area was conducted to build trust, explain the study objec-
tives, mobilize the community leaders, and ask the community to be involved in all parts of the
study. This led to a sense of ownership and empowerment. Thus, successful face-to- face inter-
views with the heads of households at their home could take place in a friendly environment.
Rift Valley fever outbreak control
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The thematic areas covered by the One Health questionnaire were socio-demographic con-
siderations, knowledge of RVF in animals and humans, attitudes and practices regarding RVF,
and environmental aspects of RVF (S1 Table).
The data were coded, entered into Microsoft Access, and checked for data entry errors by
re- entering 10% of the data from the questionnaires. The data were exported and analyzed
using STATA version 12 (Stata Corp LP. College Station, TX, USA).
Ethical statement
Ethical clearance was granted from the Ministry of Health, Gezira State, Sudan. All partici-
pants were informed about the objectives of the study and about the confidentiality of the
Fig 1. Map of Sudan. The states affected by Rift Valley fever in 2007 (Kassala, River Nile, Gezira, White Nile,
and Sennar) are indicated in yellow in the upper map. The pilot study area and the study area in Gezira State
are marked with triangles in the lower, expanded map.
doi:10.1371/journal.pntd.0005383.g001
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information and results. The participants signed an informed consent document for participa-
tion and they were free to leave the study at any time.
Results
Socio-demographic characteristics and the effect of RVF on the rural
economy
The study included slightly more women (53%) than men (47%), and almost 67% had a low
level of education (less than higher secondary school level) with no significant gender differ-
ence. Just over half (55%) were above 35 years of age, the vast majority (87%) of the heads of
households were married, and their household had at least six members (Table 1). Most
women were housewives, while men were mostly occupied with farming (Table 1).
Most of the households bred animals (72%) (Table 1). Cattle were most common, followed
by goats and sheep. Animals were kept at home (44%), near the home (22%), or far away from
home (6%). Around 25% of the households had members who worked as temporary herds-
men. Most of the households (71%) used their own livestock products as the main source of
food, and just under half (43%) sold livestock as a source of income. The 2007 RVF outbreak
negatively affected many households (46%), including disrupting the availability of food and
livestock trade for about 33% of the households.
RVF disease, transmission, protection, and sources of information
The awareness about RVF in general was high: 80% of the heads of households heard about
the disease. About 9% of the heads of households had seen people who had contracted RVF
during the 2007 outbreak. More than half of those interviewed stated that RVF is a zoonosis
that affects both animals and humans, and that RVF had been a serious health problem in the
area during the 2007 outbreak. The most common sources of information in the community
about an RVF outbreak was their social networks of relatives and friends (54%) and mass
media (23%); a less common source of information was the health system (6%) or others such
as veterinarians (5%).
Table 1. Socio-demographic characteristics of the study participants.
Category Subcategory Number (n = 235) %
Gender Male 111 47
Female 124 53
Age,years � 35 105 45
> 35 130 55
Educational Level* Low 158 67
High 77 33
Occupation** Housewife,Student,Unemployed 133 57
Farmer 55 23
Health professional/Teacher/Freelancer 47 20
Marital status Unmarried 31 13
Married 204 87
Breed animals Yes 170 72
No 65 28
*Low education is less than higher secondary school.
**The first group was lumped together during the analysis as they were all dependent in that context. The third group was lumped together during the
analysis as they were the most educated.
doi:10.1371/journal.pntd.0005383.t001
Rift Valley fever outbreak control
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According to the respondents, there was higher livestock mortality in the area during the
2007 RVF outbreak than the year before (2006) and the year after (2008) the outbreak. During
the 2007 RVF outbreak, 34% of the heads of households had experienced death of livestock; in
2006 and 2008 only 17% had experienced death of livestock. This difference, however, could
not be confirmed from official reports.
Although the community experienced higher livestock mortality, only some mentioned
known symptoms in livestock that died, such as nasal and ocular discharge and hemorrhagic
diarrhea (Table 2). Regarding sick livestock, known RVF symptoms were not mentioned by
the majority: only 20% stated hemorrhaging and less than 9% mentioned fever and refusal to
eat (Table 2). Likewise, RVF symptoms in humans were not well known to the majority of the
respondents: 25% stated that fever and hemorrhagic symptoms were most common.
Most of the respondents did not know how livestock become infected with RVF. For
human infection, (21%) stated that humans are infected through uncooked meat while 13%
suggested direct contact with livestock. Only a few respondents suggested other mode of trans-
mission such as raw milk (9%), and mosquito bites (6%). The most common answer on how
humans should avoid RVF, was to avoid uncooked meat and handling of sick livestock. Avoid-
ing livestock that had suffered miscarriage was the least important according to the results of
the survey.
Although few thought that RVF is a contagious disease, more than half of the respondents
expected to get RVF when it was present in their area―either due to animal-to-human contact
or human-to-human contact (Table 3). One-quarter said that they would avoid contact with
neighbors who they suspected of having RVF. About half of the participants (45%) were in
favor of patient isolation as a preventive measure during outbreaks and 12% stated that they
would avoid contact with RVF patients. Mosquito nets on beds were used by 60% of the
respondents, but less than half of these (40%) were impregnated. The majority (60%) had
noticed an increase in mosquito population during 2007. To prevent RVF in livestock, the
respondents suggested isolation of sick livestock (21%) and vaccination (14%). In addition, the
majority of respondents (73%) strongly recommended quarantine of RVF-infected livestock.
Table 2. Perceived RVF symptoms reported by participants regarding their livestock or livestock in
the area suspected of having RVF during the 2007 outbreak (n = 235).
Number of animals %
RVF symptoms perceived in animals with fatal disease
Nasal and ocular discharge 37 15
Do not remember 17 7
Diarrhea/hemorrhage 12 5
High fever 10 4
Abortion 10 4
RVF symptoms perceived in sick animals that survived
Hemorrhage 47 20
Do not remember 35 15
Fever 19 8
Stopped eating food 18 8
Other mixed symptoms 13 6
Digestive disorders 7 3
Note: More than one symptom was allowed.
doi:10.1371/journal.pntd.0005383.t002
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The survey revealed that two-thirds of the participants had a positive attitude about medical
treatment against RVF in humans. However, only one-third thought that medical treatment
could be used for livestock. They also indicated that veterinarians should diagnose RVF in live-
stock and health workers should diagnose RVF in human. Around 75% of the heads of house-
holds knew where to seek medical treatment, either in the public or the private health sector.
Reporting and control of an RVF outbreak
If an outbreak occurs, about 40% said they should notify the veterinary authorities about
the death of livestock. Almost all the respondents (99%) stressed that they would not get any
compensation for their dead livestock if they notified the authorities. When asked if any of
their own livestock had had RVF during the 2007 outbreak, 13% said yes. These suspected
cases were not confirmed by the authorities. When we asked which disciplines need to work
together in order to control RVF, only eight participants (3%) stated that veterinary and health
authorities should work together. The majority believed that human health authorities (50%)
rather than veterinary authorities (15%) should work to control RVF. With regard to the com-
munity’s role in confronting RVF, the respondents suggested that the community should
improve its hygienic measures (22%), its health education (18%) and its vector control (8%).
The majority of the study participants (70%) were aware that RVF could spread from one
region to another within the country. In addition, 66% of the participants revealed that they
were aware of the livestock trade ban associated with RVF outbreak inside and outside the
country.
Discussion
We used the 2007 RVF outbreak in Sudan as a case study to investigate, the knowledge, atti-
tudes and practices, from the One Health perspective that affect the involvement of the local
community in disrupting an emerging zoonotic infection. Most of the measures aimed to con-
trol RVF were formulated by authorities (i.e., health and veterinary) to be implemented by the
local communities (a top-down). For RVF, it seems as these actions are not enough as disease
emergence continues. We believed that insights from the local community (a bottom-up
approach) about RVF prevention and control could help stop the spread of RVF outbreaks.
This bottom-up approach could be a tool to better combat the transmission and the spread of
RVF in the regions where the outbreaks are initiated, and could enhance a top down approach.
To identify the important factors we used the unique One Health approach to gather informa-
tion about livestock, people, and the environment. We also investigated whether the commu-
nity considered the integration of the One Health approach of health, veterinarians, and
environment authorities as the best strategy to confront RVF and how they could contribute
to RVF control.
Table 3. Common perceived reasons as to how the participants could be infected by RVFV if spread in the area compared to what has been
reported in the literature.
Percieved reasons Number of Respondents(n = 235) % What has been reported in the literature
Person -to-person contact 94 40 Misconception by participants
We have animals 26 12 Possible if contact with sick animals
I am handling animals 11 5 Possible if animal is sick.
Get it through people coughing 5 2 Misconception by participants
Do not use mosquito bed net 3 1 Possible if bitten by an infected mosquito
Note: More than one answer was allowed.
doi:10.1371/journal.pntd.0005383.t003
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Although the community studied had experienced a large outbreak, few had proper knowl-
edge of RVF regarding cause, mode of transmission, symptoms, prevention, and control. This
lack of knowledge increases the chances of RVF spreading to neighboring areas and would
prevent the community from confronting the disease. The knowledge of risk factors for RVF
was insufficient, because the community only practiced some of the measures known to pre-
vent RVF [21] (e.g., eating cooked meat and staying away from sick livestock) while exposing
themselves to other risks (e.g., exposure to mosquitoes and handling miscarriage livestock). As
in most rural areas, these communities in rural Sudan depend on their livestock as a source of
food and income, and often breed and raise their livestock inside or near their homes [22].
The majority did not know that handling livestock that had miscarried was a serious risk factor
for RVF [23]. This lack of knowledge could pose a significant risk, especially for rural women,
as they tend to take care of livestock at home.
Although the community lives near irrigation canals, which serve as a breeding site for
mosquito vectors, the majority ignored mosquitoes as a source of infection. The lack of knowl-
edge of risk factors for transmission could explain the high number of cases reported in the
2007 RVF outbreak in Sudan [18]. Like other mosquito-borne diseases, RVF is associated with
heavy rains [23], so the authorities could update communities about rain forecasts. This
knowledge would encourage a participatory role of local communities in integrated vector
control management similar to the malaria control programs that have been established in
most countries where malaria is endemic. The infrastructure of such programs such as estab-
lished vector control management and the use of impregnated mosquitoes bed nets could also
help control other types of mosquito-borne viruses in endemic regions[24, 25].
Therefore, human behavior contributes to the disease emergence. To control the spread of
RVF, it is essential to understanding how local communities interact with livestock and the
environment. We expect that social scientists, who are well equipped to deal with human
behavior changes, will be able to find acceptable ways for rural communities to practice better
animal husbandry [26].
For control of RVF, we found the main focus in the community was human health and
access to regional hospitals, particularly in the rainy season when the roads are difficult to nav-
igate. Notably, the animal dimension to confronting a zoonosis such as RVF was not well
understood. To better implement the One Health approach, authorities could work together
with communities to prevent and control emerging zoonotic diseases. This is particularly
important because the veterinary services might not be able to cover a vast country like Sudan,
where the veterinarians are based in the capital of each locality. The veterinarians visit remote
villages for vaccination or investigation of suspected cases of abnormal livestock diseases and
visits during rainy season are very difficult due to flooded and otherwise impassable roads. In
such a context, voluntary animal health workers from the local communities could be trained
to identify livestock diseases, including RVF. This work would take place in collaboration
with veterinarians, who have an increasingly important role in global health [27]. Similarly,
human voluntary health workers could be trained to identify human diseases. These volunteers
could be selected in cooperation with community leaders, which would ensure successful
collaboration and communication between health care providers and the community. The
sustainability of such a system would depend on a rapid response and support from the
authorities when needed by the local communities. These suggestions are in keeping with a
participatory approach that regards farmers as being effective partners to curb zoonoses
[28, 29].
The rural household economy is affected by RVF outbreaks, regarding both food security
and disrupted incomes. There were two opposing interests. The community was only inter-
ested in interventions to curb the disease that would not result in the culling of livestock
Rift Valley fever outbreak control
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without compensation. The absence of a compensation system weakened the motivation to
report early cases in livestock to veterinary authority, a requirement if RVF is to be halted
before infecting humans. This lack of compensation could be a possible explanation for the
delay in reports of RVF in livestock. If RVF had been identified in livestock early, then live-
stock as well as human RVF outbreaks in Sudan in 2007 and in Kenya in 1997–1998 might
have been prevented [18, 30]. To support the devastated rural economy due to RVF outbreaks
[3], a new policy of compensation for culled or dead livestock must be developed. The respon-
dents stressed the importance of safe vaccination at the right time to prevent their livestock
from contracting RVF and preventing the spread of RVF to humans, [31]. Normally, RVF vac-
cination of livestock is not free in Sudan, an expenditure that might impede locals from regu-
larly vaccinating their livestock, bearing in mind that a new episode of RVF might take some
years to re-emerge. Therefore, subsidizing vaccinations for emerging zoonotic diseases might
encourage farmers to regularly vaccinate their livestock. In general, RVF livestock vaccines
are either inactivated or live attenuated [32, 33]. However, the inactivated vaccine needs multi-
ple doses to booster immunity, making it more expensive and more difficult to distribute.
Because the vaccine requires multiple shots, establishing immunity requires time and this vul-
nerability decreases the vaccine’s usefulness during outbreaks. The live attenuated vaccine is
administered as a single dose, but it has shown some teratogenic effects that can lead to abor-
tion among inoculated pregnant animals[34, 35]. However, safe vaccine remains the effective
way to protect animals and humans [33, 36].
The respondents were aware of the possibility of RVF spreading inside the country, espe-
cially through the free mobility livestock grazing system. They also knew about the economic
consequences of a ban on livestock trade after an RVF outbreak. This awareness is important
to consider when early warning systems are developed to avoid bias in disease surveillance.
The community’s main sources of information on RVF were social network and mass media
such as radio, not veterinarians or health workers, who were mainly involved in case notifica-
tion rather than increasing public awareness [37]. The strong dependence on social networks,
rather than on medical and veterinary professionals, could increase the risk of misconceptions
if the wrong information is spread. Thus, the World Health Organization recommends that
during zoonotic outbreaks interdisciplinary teams of health providers, veterinarians and en-
vironmentalists, provide main communication with the public [38]. These teams can com-
municate through social networks and mass media such as radio, which is one of the most
common sources of information in remote areas of many countries. This local involvement
will empower the community, allowing them to contribute to notification and control of the
outbreaks, and lead them to play proactive roles. This cooperation could strengthen the
national surveillance system, which depends mostly on passive notification, a system that
might overlook health related events in remote areas. Empowering livestock owners is an
opportunity to strengthen the surveillance system for zoonoses, including RVF [39].
Although our study was conducted in 2013 in an area that was affected during the 2007
RVF outbreak in Sudan, up-to-date questions about RVF were also asked at the time of the
study. For the questions related to the 2007 RVF outbreak, we considered recall bias. Since the
2007 RVF outbreak, no other recorded hemorrhagic fever outbreaks had occurred in this area
according to the participants, so the participants would not have mixed the information about
RVF with other similar diseases. In addition, the 2007 outbreak was severe, affecting humans,
livestock and the economy in a unique way, which made it easier to remember, decreasing the
possibility of recall bias.
In general, the results of this survey are generalizable for the agro-pastoralist regions of
Sudan due to the similarity of the context as well as for other countries that experience
endemic RVF with similar knowledge, attitudes and practices.
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Conclusions
This study addressed the challenges and opportunities of including local communities in con-
trolling RVF outbreaks at the interface between humans, animals, and their environment. The
suddenness of the outbreaks, the lack of treatment, the lack of vaccines, and the complex trans-
mission cycle of RVFV highlights the need to increase community participation in disrupting
RVF outbreaks. Crucial challenges include improving the knowledge and correcting miscon-
ceptions about RVF that result in risky behaviors. However, by empowering rural communi-
ties through education and motivating them to recognize cases early, the authorities could be
notified and could act accordingly to support the local community. The willingness of the
community to participate in curbing RVF outbreaks is an opportunity that can be effectively
managed in a bottom-up approach: the more we know about a community’s knowledge, atti-
tudes and practices related to the emergence of RVF, the better we will be embowering local
communities with the best information and strategies to prevent the spread of RVF. That is,
this bottom-up approach may result in mutually acceptable and cost-effective interventions
that can be used to disrupt transmission of RVF in affected communities.
Supporting information
S1 Checklist.
(DOC)
S1 Table. One Health questionnaire.
(DOCX)
Acknowledgments
We are grateful to the Ministry of Health, Gezira State, Sudan for facilitating the study. We
thank the community and the community leaders in the pilot and study areas for their kind
collaboration. We are also grateful to the data collectors. We also thank Dr. Rania Salah Eldin
Bashir Abass for kind help with Fig 1.
Author Contributions
Conceptualization: OAH CA JR HA RS ME.
Data curation: OAH PM.
Formal analysis: ME OAH.
Funding acquisition: ME.
Investigation: OAH.
Methodology: ME CA JR RS HA OAH.
Project administration: OAH ME.
Resources: OAH PM.
Writing – original draft: OAH PM HA JR RS CA ME.
References1. Woods CW, Karpati AM, Grein T, McCarthy N, Gaturuku P, Muchiri E, et al. An outbreak of Rift Valley
fever in northeastern Kenya, 1997–98. Emerging infectious diseases. 2002; 8(2):138–44. doi: 10.3201/
eid0802.010023 PMID: 11897064
Rift Valley fever outbreak control
PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0005383 February 16, 2017 10 / 12
2. Hassan OA, Ahlm C, Evander M. A need for One Health approach-lessons learned from outbreaks of
Rift Valley fever in Saudi Arabia and Sudan. Infection ecology & epidemiology. 2014; 4.
3. Peyre M, Chevalier V, Abdo-Salem S, Velthuis A, Antoine-Moussiaux N, Thiry E, et al. A Systematic
Scoping Study of the Socio-Economic Impact of Rift Valley Fever: Research Gaps and Needs. Zoono-
ses and public health. 2015; 62(5):309–25. doi: 10.1111/zph.12153 PMID: 25256804
4. Anholt R, Stephen C, Copes R. Strategies for collaboration in the interdisciplinary field of emerging zoo-
notic diseases. Zoonoses and public health. 2012; 59(4):229–40. doi: 10.1111/j.1863-2378.2011.
01449.x PMID: 22273426
5. Zinsstag J, Mackenzie JS, Jeggo M, Heymann DL, Patz JA, Daszak P. Mainstreaming one health. Eco-
Health. 2012:1–4.
6. Zinsstag J, Schelling E, Waltner-Toews D, Tanner M. From “one medicine” to “one health” and systemic
approaches to health and well-being. Preventive veterinary medicine. 2011; 101(3):148–56.
7. Greter H, Jean-Richard V, Crump L, Bechir M, Alfaroukh IO, Schelling E, et al. The benefits of’One
Health’for pastoralists in Africa. Onderstepoort Journal of Veterinary Research. 2014; 81(2):1–3.
8. Preston ND, Daszak P, Colwell RR. The human environment interface: applying ecosystem concepts to
health. One Health: The Human-Animal-Environment Interfaces in Emerging Infectious Diseases:
Springer; 2013. p. 83–100.
9. Shope R, Peters C, Davies F. The spread of Rift Valley fever and approaches to its control. Bulletin of
the World Health Organization. 1982; 60(3):299. PMID: 6982772
10. Baudin M, Jumaa AM, Jomma HJ, Karsany MS, Bucht G, Naslund J, et al. Association of Rift Valley
fever virus infection with miscarriage in Sudanese women: a cross-sectional study. The Lancet Global
Health. 2016; 4(11):e864–e71. doi: 10.1016/S2214-109X(16)30176-0 PMID: 27692776
11. Gerdes G. Rift valley fever. Revue scientifique et technique-Office International des Epizooties. 2004;
23(2):613–24.
12. Nanyingi MO, Munyua P, Kiama SG, Muchemi GM, Thumbi SM, Bitek AO, et al. A systematic review of
Rift Valley Fever epidemiology 1931–2014. Infection ecology & epidemiology. 2015;5.
13. Ahmad K. More deaths from Rift valley fever in Saudi Arabia and Yemen. The Lancet. 2000; 356
(9239):1422.
14. Chevalier V. Relevance of Rift Valley fever to public health in the European Union. Clinical Microbiology
and Infection. 2013; 19(8):705–8. doi: 10.1111/1469-0691.12163 PMID: 23517372
15. Rolin AI, Berrang-Ford L, Kulkarni MA. The risk of Rift Valley fever virus introduction and establishment
in the United States and European Union. Emerging microbes & infections. 2013; 2(12):e81.
16. Turell MJ, Dohm DJ, Mores CN, Terracina L, Wallette DL Jr, Hribar LJ, et al. Potential for North Ameri-
can Mosquitoes to Transmit Rift Valley Fever Virus1. Journal of the American Mosquito Control Associ-
ation. 2008; 24(4):502–7. doi: 10.2987/08-5791.1 PMID: 19181056
17. Moutailler S, Krida G, Schaffner F, Vazeille M, Failloux A-B. Potential vectors of Rift Valley fever virus in
the Mediterranean region. Vector-borne and zoonotic Diseases. 2008; 8(6):749–54. doi: 10.1089/vbz.
2008.0009 PMID: 18620510
18. Hassan OA, Ahlm C, Sang R, Evander M. The 2007 rift valley fever outbreak in Sudan. PLoS Negl Trop
Dis. 2011; 5(9):e1229. doi: 10.1371/journal.pntd.0001229 PMID: 21980543
19. Sudan Seasonal Monitor [cited October 2016 21]. Available from: http://www.fao.org/fileadmin/user_
upload/emergencies/docs/Sudan_seasonal_monitor_Nov07.pdf.
20. Gezira Ministry of Health-Epidemiologic Report 2008.
21. Nicholas DE, Jacobsen KH, Waters NM. Risk factors associated with human Rift Valley fever infection:
systematic review and meta-analysis. Tropical Medicine & International Health. 2014; 19(12):1420–9.
22. Brown H, Kelly AH, Saez AM, Fichet-Calvet E, Ansumana R, Bonwitt J, et al. Extending the “Social”:
Anthropological Contributions to the Study of Viral Haemorrhagic Fevers. PLoS Negl Trop Dis. 2015; 9
(4):e0003651. doi: 10.1371/journal.pntd.0003651 PMID: 25880853
23. Davies F, Linthicum K, James A. Rainfall and epizootic Rift Valley fever. Bulletin of the World Health
Organization. 1985; 63(5):941. PMID: 3879206
24. Walker K, Lynch M. Contributions of Anopheles larval control to malaria suppression in tropical Africa:
review of achievements and potential. Medical and veterinary entomology. 2007; 21(1):2–21. doi: 10.
1111/j.1365-2915.2007.00674.x PMID: 17373942
25. Goodman CA, Coleman PG, Mills AJ. Cost-effectiveness of malaria control in sub-Saharan Africa. The
Lancet. 1999; 354(9176):378–85.
26. Lapinski MK, Funk JA, Moccia LT. Recommendations for the role of social science research in one
health. Social Science & Medicine. 2015; 129:51–60.
Rift Valley fever outbreak control
PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0005383 February 16, 2017 11 / 12
27. Kelly A, Osburn B, Salman M. Veterinary medicine’s increasing role in global health. The Lancet Global
Health. 2014; 2(7):e379–e80. doi: 10.1016/S2214-109X(14)70255-4 PMID: 25103380
28. Catley A, Alders RG, Wood JL. Participatory epidemiology: approaches, methods, experiences. The
Veterinary Journal. 2012; 191(2):151–60. doi: 10.1016/j.tvjl.2011.03.010 PMID: 21856195
29. Goutard FL, Binot A, Duboz R, Rasamoelina-Andriamanivo H, Pedrono M, Holl D, et al. How to reach
the poor? Surveillance in low-income countries, lessons from experiences in Cambodia and Madagas-
car. Preventive veterinary medicine. 2015; 120(1):12–26. doi: 10.1016/j.prevetmed.2015.02.014 PMID:
25842000
30. Centers for Disease Control and Prevention. Rift Valley Fever—East Africa, 1997–1998. MMWR Mor-
bidity and mortality weekly report. 1998; 47(13):261. PMID: 9565487
31. Bird BH, Nichol ST. Breaking the chain: Rift Valley fever virus control via livestock vaccination. Current
opinion in virology. 2012; 2(3):315–23. doi: 10.1016/j.coviro.2012.02.017 PMID: 22463980
32. World Organization for Animal Health (OIE). Rift Valley Fever- Manual of Diagnostic Tests and Vac-
cines for Terrestrial Animals-Chapter 2.1.18 [cited August 2016 12]. Available from: http://www.oie.int/
fileadmin/Home/eng/Health_standards/tahm/2.01.18_RVF.pdf
33. Ikegami T, Makino S. Rift valley fever vaccines. Vaccine. 2009; 27:D69–D72. doi: 10.1016/j.vaccine.
2009.07.046 PMID: 19837291
34. Sall A, Zanotto PdA, Vialat P, Sene O, Bouloy M. Molecular epidemiology and emergence of Rift Valley
fever. Memorias do Instituto Oswaldo Cruz. 1998; 93(5):609–14. PMID: 9830526
35. World Organization for Animal Health(OIE). Animal Diseases Information-Rift Valley fever-Fact Sheet.
2016 [cited August 2016 06]. Available from: http://www.oie.int/fileadmin/Home/eng/Media_Center/
docs/pdf/Disease_cards/RVF-EN.pdf.
36. Kortekaas J, Zingeser J, de Leeuw P, de La Rocque S, Unger H, Moormann RJ. Rift Valley fever vac-
cine development, progress and constraints. Emerging infectious diseases. 2011; 17(9):e1. doi: 10.
3201/eid1709.110506 PMID: 21888781
37. Rehima MME, Abdelgadir AE, ELMalik KH. Raising community awareness about Zoonotic diseases
with special reference to rift valley fever, the roles of professionals and media. Journal of Cell and Ani-
mal Biology. 2011; 5(14):299–307.
38. Diallo M, Nabeth P, Ba K, Sall A, Ba Y, Mondo M, et al. Mosquito vectors of the 1998–1999 outbreak of
Rift Valley Fever and other arboviruses (Bagaza, Sanar, Wesselsbron and West Nile) in Mauritania and
Senegal. Medical and veterinary entomology. 2005; 19(2):119–26. doi: 10.1111/j.0269-283X.2005.
00564.x PMID: 15958020
39. Butcher N, Tan M, Sheikh M. Rift Valley fever in the Horn of Africa: challenges and opportunities. Jour-
nal of Public Health in Africa. 2012; 3(2):24.
Rift Valley fever outbreak control
PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0005383 February 16, 2017 12 / 12